Temporal persistence and structural organization of neuronal avalanche dynamics

Abstract

Brain activity can be understood as a sequence of neuronal avalanches, i.e., transient episodes of coordinated activation that emerge across scales, from individual neurons and local networks to whole-brain dynamics. Avalanches are typically characterized by features such as size, duration, number of active components, and the silent time separating consecutive events. Although these features have been extensively characterized through their marginal distributions, their temporal organization and dependence on the underlying brain architecture remain poorly understood, leaving us without a framework for embedding neuronal avalanches within slower brain dynamics. Here, we analyzed eyes-closed resting-state magnetoencephalography recordings and the corresponding structural connectomes from 30 healthy participants to investigate the dynamics of avalanche sizes and silent times. We found that large avalanches preferentially followed short silent times, whereas small avalanches were more likely to occur after long silent periods. Based on the empirical joint distributions of avalanche size and silent time, we could define four types of events occurring above chance levels (avalanche large or small, preceding pause long or short). Mixed categories, combining a small value of one feature with a large value of the other, occurred more frequently than expected, while same-category events happened less often than chance. Furthermore, consecutive events tended to remain in the same category, a phenomenon referred to as persistence. We next investigated whether a brain region's connectivity profile shapes its propensity to participate in avalanches of different sizes. More strongly connected regions participated most often in small avalanches, whereas weakly connected regions were preferentially recruited during large avalanches. This pattern may reflect the greater sensitivity of highly connected hubs to fluctuations propagating through the network, resulting in frequent but spatially contained events. By contrast, the recruitment of more peripheral regions may require broader and stronger collective activity, occurring only during rarer, large-scale avalanches. In contrast, regional participation showed no clear association with the silent time preceding an avalanche. Together, these findings show that neuronal avalanches are neither temporally independent nor anatomically unconstrained: their sequence retains a memory of preceding events, while structural topology shapes which regions are recruited as avalanches grow. By connecting avalanche dynamics with slower temporal organization and the structural connectome, our results provide a multiscale framework for understanding how transient events are embedded within ongoing brain activity.